Abstract
Dimethylsulfoniopropionate (DMSP), an osmolyte produced by oceanic phytoplankton and bacteria, is primarily degraded by bacteria belonging to the Roseobacter lineage and other marine Alphaproteobacteria via DMSP-dependent demethylase A protein (DmdA). To date, the evolutionary history of DmdA gene family is unclear. Some studies indicate a common ancestry between DmdA and GcvT gene families and a co-evolution between Roseobacter and the DMSP-producing-phytoplankton around 250 million years ago (Mya). In this work, we analyzed the evolution of DmdA under three possible evolutionary scenarios: (1) a recent common ancestor of DmdA and GcvT, (2) a coevolution between Roseobacter and the DMSP-producing-phytoplankton, and (3) an enzymatic adaptation for utilizing DMSP in marine bacteria prior to Roseobacter origin. Our analyses indicate that DmdA is a new gene family originated from GcvT genes by duplication and functional divergence driven by positive selection before a coevolution between Roseobacter and phytoplankton. Our data suggest that Roseobacter acquired dmdA by horizontal gene transfer prior to an environment with higher DMSP. Here, we propose that the ancestor that carried the DMSP demethylation pathway genes evolved in the Archean, and was exposed to a higher concentration of DMSP in a sulfur-rich atmosphere and anoxic ocean, compared to recent Roseobacter eco-orthologs (orthologs performing the same function under different conditions), which should be adapted to lower concentrations of DMSP.
Highlights
Dimethylsulfoniopropionate (DMSP) is an osmolyte synthesized by oceanic phytoplankton (Galinski, 1995; Yoch, 2002)
We identify a total of 204 DmdA protein sequences out of 150 curated genomes, and reconstruct their evolutionary relationships by Bayesian Inference (BI) (Fig 1) and Maximum Likelihood (ML)
When we tested the intensity of selection over evolutionary time using the free-ratio model (Table 4), we found changes in the selection pressure from the branches which defines the separation of SAR11 and Roseobacter DmdA gene families (Supplementary Fig 19: branches from nodes 21 to 23)
Summary
Dimethylsulfoniopropionate (DMSP) is an osmolyte synthesized by oceanic phytoplankton (Galinski, 1995; Yoch, 2002) This molecule became abundant in the oceans 250 million years ago (Mya), coinciding with the expansion and diversification of dinoflagellates (Bullock et al, 2017). Since it has played an important role in the biogeochemistry of sulfur cycle on Earth (Lovelock, 1983). Candidatus Pelagibacter ubique (SAR11), dominant in the bacterioplankton and especially in surface waters, can only use sulfur atoms derived organic molecules, such as DMSP (Tripp et al, 2008). In the case of Ruegeria pomeroyi DSS-3, a model organism for DMSP studies, the turnover rate of DMSP transformation depends on salinity conditions (Salgado et al, 2014)
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